Discussion
Ecosystem processes interact via exerting trade-offs or legacy effects (Reich 2014). Disentangling the linkages among processes could improve the predictive and mechanistic understanding of nutrient-cycling responses to changing environments (Cornwell et al. 2008). For the first time, we integrated the vertical (belowground nutrient absorption vs aboveground nutrient resorption) and temporal processes (nutrient flows from green leaf to senesced leaf to leaf litter) associated with the whole-plant nutrient economy among 15 subtropical tree species. Nutrients in new leaves are from two pathways: root absorption from soil (‘Get’) and resorption from senesced leaves (‘Save’) (Wright & Westoby 2003). We found that root nutrient absorption potential was negatively correlated with leaf nutrient resorption proficiency (Fig. 2a), indicating a cost-benefit trade-off between belowground absorption and aboveground resorption in nutrient acquisition pathways (Wright & Westoby 2003). Such an economic trade-off has further caused a legacy effect on subsequent leaf-litter decomposition (‘Return’) as indicated by the negative relationship between nutrient resorption proficiency and mass loss rate (Fig. 2a). The active trade-off between absorption and resorption as well as the passive trade-off between resorption and decomposition jointly indicate the existence of the ‘GSR’ continuum.
The continuum centred primarily on the P economy when examining the specific nutrients. The PAP was negatively correlated with PRP (P= 0.048; Fig. 2a), indicating that greater root nutrient absorption can lead to an increased P concentration in leaf litter (i.e. decreased PRP). Meanwhile, P concentration in leaf litter was positively correlated (i.e. PRP was negatively correlated) with the decomposition rate (P = 0.035; Fig. 2a). The resorption proficiency rather than efficiency that emerged in these linkages supports the argument that selection acts upon the residual nutrient concentration in senesced leaves rather than proportional resorption per se (Killingbeck 1996; Wright & Westoby 2003). The allocation of effort toward nutrient absorption and resorption depends on both soil nutrient availability and the cost involved in these processes (Kou et al. 2017). The continuity of the P economy could be related to the local edaphic conditions, where soil P availability (6.54 mg kg-1; Table S3) is relatively low compared to the global level (Zhu et al. 2016). For example, lower P availability can enhance root nutrient foraging strategies (Kou et al. 2018b; Li et al. 2019) and retard leaf-litter decomposition (Jiang et al. 2018, 2019) in P-deficient subtropical forests. Considering that nutrients obtained via resorption also incur a cost, e.g. the hydrolysis of organic compounds (Norby et al. 2000), plants should make an active trade-off between nutrient acquisition pathways by decreasing P resorption (i.e. saving less nutrients) for cost saving.
These processes associated with the N economy were not well linked, as indicated by the decoupling between NAP and NRP (P > 0.05; Fig. 2a). The discontinuity in the N economy supports our hypothesis that the continuum is mainly determined by the trade-off between the two nutrient acquisition pathways. The trade-off disappearance was possibly because N may not be the most limiting nutrient in N-rich subtropical soils (Kou et al. 2018a). The discontinuity may alternatively be related to the diverse forms of N. Unlike P, which is exported in inorganic form (Vance et al. 2003), N can be exported in a diverse array of inorganic and organic forms (Takebayashi et al. 2010). In contrast to ammonium, which must be assimilated in roots, nitrate can be absorbed into organic compounds in roots and leaves (Wang & Macko 2011; Zhou et al. 2020). The dual pathways of nitrate assimilation might influence the assessment of root absorption and leaf resorption, obscuring their linkages. Like the P economy, NRP was marginally negatively correlated with decomposition rate (P = 0.052; Fig. 2a), consistent with a recent study showing linkages between leaf nutrient resorption and litter decomposition (Xu et al. 2020). This is unsurprising because the initial nutrient chemistry of leaf litter is closely associated with resorption (Deng et al. 2018) and inherently determines decomposition rates at the local scale (Cornwell et al. 2008).
The continuum conformed to the economics spectrum theory, when linking LES to ‘GSR’ continuum (Fig. 4). The one-dimensional ‘fast-slow’ LES, capturing a suite of key traits, represents species strategies as shaped by their evolutionary history (Reich et al. 1997; Wright et al. 2004) and assumes that the acquisitive-strategy species live fast and die young, while the conservative-strategy species live slow and steady (Wright et al. 2004). We correlated the PC1 scores on the LES with these processes, and found that species at the fast end of the spectrum had higher PAP (R 2 = 0.27, P = 0.047; Fig. 4a) and litter P concentration (R 2 = 0.50,P = 0.003; Fig. 4b), while species at the slow end presented the opposite patterns. These results indicate that species at both ends of the LES have contrasting investment strategies regarding nutrient acquisition: acquisitive-strategy species rely more on nutrient absorption but less on nutrient resorption compared to the conservative-strategy species. Less resorption for the acquisitive-strategy species yielded higher-quality leaf litter, and thus faster decomposition (R 2 = 0.39, P= 0.013; Fig. 4c). Such a passive trade-off implies that selection acts not only upon resorption but also upon decomposability by influencing the residual nutrient concentration in senesced leaves. These findings jointly suggest that the trait-based LES can be extrapolated to the process-based ‘GSR’ continuum.
Nutrient return via decomposition provides feedback to the soil matrix and may, in turn, influence root absorption. Perennial plants colonising a habitat may deploy nutrient foraging strategies in multiple dimensions, such as the ‘afterlife’ strategy—decomposition. Based on root trait-decomposition linkages, we found that the acquisitive-strategy species have thinner absorptive roots, but slower root decomposition compared to the conservative-strategy species (Jiang et al. 2021). This finding suggests a potential trade-off between absorptive-root turnover (diameter as a proxy) and decomposition and a possible belowground mechanism underlying species coexistence (Jiang et al. 2021). Despite this, there was no direct link between root absorption and leaf-litter decomposition on the ‘GSR’ continuum (P > 0.05; Fig. S3), implying that fast decomposition may not enable the acquisitive-strategy species to preempt the returned nutrients. This asymmetry could be related to two causes. First, leaf litter can decompose away from the home field under physical forces from wind or forest animals (Veen et al. 2019). Second, soil microorganisms or neighbouring plants may compete for and immobilise the returned nutrients (Barbe et al. 2017), which impels the acquisitive-strategy species to run steadily in a fast lane.
The ‘GSR’ continuum running on P economy emerged among ECM species rather than AM species (Fig. 4), supporting our hypothesis that the continuum varied with mycorrhizal type. The contrasting patterns between mycorrhizal types could be because ECM species generally dominate in ‘slow-cycling’ ecosystems with nutrient conservative traits, while AM species dominate ‘fast-cycling’ ecosystems with nutrient acquisitive traits (Philips et al. 2013). Compared to AM species, ECM species may have a strict budget for C investment and thus a tight linkage between root absorption and leaf resorption. Furthermore, AM and ECM species have different degrees of dependence on mycorrhizal fungi based on the root-fungal collaboration gradient globally (Bergmann et al. 2020). From absorptive-root trait comparisons between AM and ECM species, we found that ECM species had greater BI and SRL (marginally significant), and AM species had higher RD (Table 1). These divergences in root traits implied that AM species rely more on mycorrhizal symbiosis, while ECM species rely more on roots themselves when acquiring the limiting nutrients (Bergmann et al. 2020). Therefore, the two pathways of nutrient acquisition could be coupled for the more self-dependent ECM species compared to the more symbiosis-dependent AM species.
While leaf nutrient resorption and leaf-litter decomposition are negatively correlated (Xu et al. 2020), it remains unclear whether the trade-off between the two processes depends on the mycorrhizal type. By partitioning all species into two mycorrhizal groups, we found a tight linkage between these two processes among ECM species (P = 0.022; Fig. 2c) rather than AM species (P > 0.05; Fig. 2b). This divergent pattern may be related to the contrasting trait controls over leaf-litter decomposition in AM and ECM species (Phillips et al. 2013). Leaf-litter decomposition of ECM species was associated more closely with chemical traits (N and P) (Table S4). In contrast, decomposition of AM species was more correlated with morphological traits (e.g. SLA and LTD; Table S4) rather than chemical traits, although the ‘fast-slow’ LES was linked to decomposition in AM species (Fig. 4c). Despite these findings, the limited number of species makes it difficult to draw robust conclusions when taking a closer look at the mycorrhizal type, although AM (n = 8) and ECM (n = 7) species were comparable in terms of sample size. Studies incorporating more mycorrhizal tree species are therefore needed to further examine these active and passive trade-offs between nutrient-associated processes.
Overall, our results suggest that there was an active trade-off between root P absorption and leaf P resorption, which caused a passive trade-off between leaf P resorption and leaf-litter decomposition. Based on these findings, we conclude that the ‘GSR’ continuum exists and runs on the P economy among these subtropical tree species, providing a predictive framework for the whole-plant nutrient economy. Importantly, we linked the ‘fast-slow’ leaf economics spectrum to the processes associated with tree nutrient economy on this continuum and revealed that species with acquisitive leaf traits have greater root P absorption, lower leaf P resorption, and faster leaf-litter decomposition, while species with conservative leaf traits presented opposite patterns. These findings imply that the ‘fast-slow’ leaf economics spectrum can be extended to the process-based ‘GSR’ continuum and advance our understanding of the adaptive strategies of acquisitive and conservative species at multi-dimensional scales. Furthermore, the ‘GSR’ continuum emerged among ECM species rather than AM species, demonstrating the importance of mycorrhizal symbiosis in regulating the tree nutrient economy.